Applying error management theory to understand the evolution of decision-making in plant defense

尽管植物以被动著称，但就像动物一样，它们进化出了一种非凡的能力，能够感知和回应有关其环境中威胁的信息。然而，与动物不同的是，植物如何对不同的信息进行优先排序并评估风险，以便就如何应对做出决定，这一点尚不清楚。这项研究项目将使用错误管理理论来评估高大的黄花植物(Solidago Altissima)如何根据它们从环境中接收到的线索来评估草食威胁。我们已经知道，在食草动物到达之前，高大黄花可以感知并响应两种不同的空中线索来启动防御：(1)来自关键的破坏性草食物种的吸引配偶的化学物质(信息素)；(2)从邻近的高大黄花植物释放的挥发性化学物质，这些化学物质正受到通才昆虫的攻击。将进行温室和田间实验，以确定线索阈值，不同线索触发哪些基因，以及当线索与收到的损伤类型匹配或不匹配时做出反应的成本和收益。最终，在没有做出反应的情况下犯下错误的代价将通过草食动物受到损害而导致的生殖产出减少来衡量。结果将揭示高大黄花是否采取了一种押注对冲的方法，并分配了防御措施，以将代价高昂的错误降至最低，从而有利于减少代价较低的错误。通过从这个新的角度探索植物防御，这项研究将极大地拓宽我们对植物如何做出决定的理解，并为植物抵御食草动物的进化提供洞察力。植物和食草动物之间的相互作用是陆地生态系统的支柱，因此了解植物如何‘决定’保护自己的应用范围从作物保护到入侵物种的控制。该项目将支持对学生和博士后研究人员的培训和指导，以及通过宾夕法尼亚州立大学建立的项目开展的公共宣传活动。高山一枝黄花是已知的少数几种植物之一，它们可以检测到并改变其防御系统，以响应两种挥发性化学信号：一种来自邻近植物，另一种来自关键的专业食草动物的交配活动。温室和田间实验将测试错误管理理论，以阐明在暴露于与关键食草动物伤害匹配和不匹配的线索后，高山毛虫不同基因型防御策略的成本和收益。随后对这些实验中的植物组织进行的植物激素和转录分析将确定在暴露于线索和虫害后基因类型的防御反应的关键机制。在各种实验情景下，针对食草动物的基因类型防御反应的有效性将揭示进化选择压力，这种压力鼓励植物尽量减少对虚假警报或昆虫的反应，而这些错误警报或昆虫不会造成实质性损害，从而降低适合度，同时优先考虑对更具破坏性的敌人的反应。该项目的研究将为植物防御如何进化以应对多种威胁提供关键见解，并具有极大的潜力为新管理策略的发展提供信息，同时提供一个有趣的主题，帮助初中生、高中生和普通公众了解常见植物和昆虫物种之间化学通信的新颖性和重要性。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势和更广泛的影响审查标准进行评估，被认为值得支持。

Despite their reputation for passivity, plants, like animals, have evolved a remarkable capacity to perceive and respond to information about threats in their environment. Unlike animals, however, it is unknown how plants prioritize different information and assess risk to 'make decisions' about how to respond. This research project will use error management theory to evaluate how tall goldenrod plants (Solidago altissima) assess threats of herbivory from cues that they receive from the environment. It is already known that tall goldenrod can perceive and respond to two different airborne cues to initiate defenses before herbivores arrive: (1) a mate-attracting chemical (pheromone) from a key damaging herbivore species and (2) volatile chemicals released from neighboring tall goldenrod plants that are being attacked by generalist insects. Greenhouse and field experiments will be conducted to determine cue thresholds, what genes are triggered by different cues, and the costs and benefits of responding when cues are matched versus mismatched with the type of damage received. Ultimately the cost of making an error in not responding will be measured by reduced reproductive output due to herbivore damage. The results will reveal whether tall goldenrod takes a bet-hedging approach and allocates defenses to minimize costly errors in favor of less costly errors. By exploring plant defenses from this novel perspective, this research will significantly broaden our understanding of how plants make decisions and provide insight on the evolution of plant defenses against herbivores. Interactions between plants and herbivores are the backbone of terrestrial ecosystems, so understanding how plants 'decide' to defend themselves has applications from crop protection to control of invasive species. The project will support training and mentorship of students and a postdoctoral researcher, as well as public outreach initiatives through established programs at The Pennsylvania State University.Solidago altissima is among the few plant species known to detect and alter its defenses in response to two volatile chemical cues: one from neighboring plants, one from the mating activity of a key, specialist herbivore. Greenhouse and field experiments will test error management theory to elucidate costs and benefits of the defensive strategies of genotypes of S. altissima following exposure to cues that are matched and mismatched with key herbivore damage. Subsequent phytohormone and transcriptomic analyses of plant tissue from these experiments will identify key mechanisms underlying defense responses of the genotypes following exposure to cues and insect damage. Under the various experimental scenarios, the effectiveness of defense responses of the genotypes against herbivores will reveal evolutionary selection pressures that have encouraged plants to minimize responses to false alarms or insects that do not do substantial damage that would reduce fitness, while prioritizing responses against more damaging foes. The research from this project will provide key insight into how plant defenses evolved to handle multiple threats and has significant potential to inform development of novel management tactics while providing an intriguing topic that will help engage middle- and high-school students and the general public in the novelty and significance of chemical communication between common plant and insect species.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.